YEARBOOK OF PHYSICAL ANTHROPOLOGY 54:47–62 (2011)

Dental Evidence for the Diets of Plio-Pleistocene Hominins

Peter S. Ungar*

Department of Anthropology, University of Arkansas, Fayetteville, AR 72701

KEY WORDS Australopithecus; Paranthropus; Homo; molar; incisor

ABSTRACT Diet is fundamental to the interaction vide evidence for the physical properties of the foods to between an organism and its environment, and is there- which a species was adapted. Dental microwear can offer fore an important key to understanding ecology and evo- insights into the properties of foods that an individual lution. It should come as no surprise then that paleoan- ate on a day-to-day basis. Taken together, these lines of thropologists have put a great deal of effort into recon- evidence can offer important insights into early hominin structing the diets of Plio-Pleistocene hominins. Most of food choices and adaptations. New methods of analysis this effort has focused on teeth; these durable parts of and theoretical perspectives are improving our under- the digestive system are usually the most commonly pre- standing of the diets of Australopithecus, Paranthropus, served elements in vertebrate fossil assemblages. In this and early Homo, and promise further progress article, I review much of this work. Tooth size, occlusal long into the future. Yrbk Phys Anthropol 54:47–62, morphology, enamel thickness, and microstructure pro- 2011. VC 2011 Wiley Periodicals, Inc.

The role of diet in human evolution is of interest to our knowledge (Ungar, 2007b). Because individuals have paleoanthropologists and laypersons alike. Most peo- different food preferences and access to different resour- ple are introduced to the subject in popular diet ces in different places and at different times, there was books. Atkins (2002) The New Diet Revolution for no single menu for a fossil hominin species, no ‘‘nutri- example, described the early hominin, ‘‘eating the fish tional contents’’ labels for us to decipher. But there are and animals that scampered and swam around him, aspects of diet we can infer. And I am convinced that we and the fruits and vegetables and berries that grew can do better than Begun’s (2004) pessimistic lamenta- nearby.’’ While such assertions offer little insight to tion that, ‘‘while it is frustrating to be unable to describe the target audience of the Yearbook of Physical An- a fossil hominoid’s behavior with sufficient detail to be thropology, The New Diet Revolution sold more than able to distinguish it from an edentate, that is probably 15 million copies. And the chapter on hominin diets as good as it gets.’’ in Sears’ (1995) New York Times #1 best seller The Most research on early hominin diets has focused on Zone has undoubtedly been read by millions more fossil teeth. Teeth are usually the most commonly pre- than even the best-cited academic paper on the same served elements in fossil assemblages, and they are the subject. The basic idea is that many chronic degener- only durable parts of the digestive system that contact ative diseases result from a discordance between our food. Teeth are especially important from an ecological biology and the foods we eat because human evolution perspective, as they are positioned at an interface funda- has not kept pace with changes in diet and other mental to the interaction between vertebrates and their aspects of lifestyle (Eaton and Konner, 1985). While environments. As the early naturalist Georges Cuvier is paleoanthropologists are unlikely to solve obesity and quoted to have said, ‘‘montrez-moi vos dents et je vous other healthcare problems any time soon, it is not dif- dirai qui vous eˆtes.’’ ‘‘Show me your teeth and I will tell ficult to understand public interest in the question, you who you are.’’ ‘‘what did early hominins eat?’’ Teeth offer vertebrate paleontologists many different But what explains interest in hominin diets among lines of evidence for reconstructing diet, both those academics? Brillat-Savarin (1825) wrote nearly two cen- related to species-level adaptations, and traces of actual turies ago, ‘‘dis-moi ce que tu manges, je te dirai qui tu use by individuals in life (see Ungar, 2010 for review). es.’’ ‘‘Tell me what you eat, I will tell you who you are.’’ The size, shape, internal architecture, and microstruc- Diet defines us, not just as individuals, but as a spe- ture of a tooth reflect natural selection for efficient ac- cies. And changing diets are surely an important key to understanding hominin evolution. Our food choices dic- tate our fundamental interactions with the environment Grant sponsors: US National Science Foundation; LSB Leakey and, as Fleagle (1999) has written, diet is ‘‘the single Foundation. most important parameter underlying the behavioral and ecological differences among living primates.’’ *Correspondence to: Peter Ungar, Department of Anthropology, Old Main 330, University of Arkansas, Fayetteville, AR 72701. Reconstructions of diet are therefore crucial to paleoan- E-mail: [email protected] thropology; they hold the potential to yield substantial insights into early hominin ecology and evolution. DOI 10.1002/ajpa.21610 We will likely never get at all the details of hominin Published online in Wiley Online Library paleonutrition; there are intractable, intrinsic limits to (wileyonlinelibrary.com).

VC 2011 WILEY PERIODICALS, INC. 48 P.S. UNGAR quisition and processing of foods with specific physical gorillas have a much lower incisor–molar size index, pre- properties. Stable isotopes in a tooth, and use-related sumably reflecting ‘‘a diet low in fruit but high in coarse damage and wear tell us about chemical and structural vegetable matter.’’ These results were consistent with properties of foods eaten by the very animal whose Robinson’s original interpretations, as Australopithecus remains are being studied. In this article, I will review had a similar incisor–molar index to gorillas, and Para- approaches that paleoanthropologists take to recon- nthropus had even smaller incisors and larger molars. structing diets of Plio-Pleistocene hominins using tooth Interestingly, Homo habilis had an incisor–molar index size, shape, structure, and wear (see Lee-Thorp and in the range of chimpanzees and orangutans. Sponheimer, 2006 for a review of tooth chemistry). Soon after, Jolly (1970) developed his seed-eater hy- Academic interest in Plio-Pleistocene hominin diets pothesis based on analogy with the gelada, a large-bod- has grown hand-in-hand with new theoretical perspec- ied, terrestrial savanna dweller with precision grip, rela- tives and methods of analysis over the past couple of tively small incisors, and large molars. He suggested decades. Today we address questions I could not have that Paranthropus dental proportions related to an ad- imagined asking in my first published review of the aptation to consume small, tough seeds. Smaller incisors subject (Ungar, 1992). Were early hominins dietary spe- were attributed to a somatic-budget effect wherein selec- cialists or generalists? How versatile were their pal- tion favors the smallest size consistent with function, ates? Do adaptations reflect selection for favored foods and the Oppenheimer effect, wherein stress limits alveo- or less preferred fallback items? These questions are lus development and room for anterior teeth (see made possible in large part by the development of Jungers 1978). Paranthropus was said to have achieved increasingly sophisticated ways of teasing more and a stable adaptive plateau (his Phase I), whereas Austral- more information from teeth. Each line of evidence can opithecus and Homo had increased incisor–molar size provide important insights as we colligate the genetic ratios, and evolved in to a Phase II omnivorous dietary and nongenetic clues. adaptation.

DENTAL ALLOMETRY Incisor allometry Researchers have long considered tooth size an impor- Work on tooth size that has followed has considered tant line of evidence of early hominin diets. The lengths the front and back teeth separately, as ratios of the two and breadths of teeth are easy to measure, species differ cannot tell us whether selection is acting on the incisors, from one another in these measurements, and logic dic- molars, or both. Hylander’s (1975) study on anthropoid tates that these differences should relate to variation in incisors provides a case in point. He found that residuals food acquisition and processing. from a regression line of incisor row width plotted against body mass reflect diet such that frugivorous cer- Early work on incisor–molar size ratios copithecines have relatively larger front teeth than do folivorous colobines (see also Goldstein et al., 1978). Fur- Robinson (1954) noted in his seminal paper on South ther, frugivorous squirrel monkeys, lar gibbons, and African hominin dentitions that ‘‘Australopithecinae’’ in chimpanzees have relatively larger front teeth than do general, and Paranthropus robustus in particular, had more folivorous howlers, siamangs, and gorillas respec- small anterior teeth compared with their cheek teeth. tively. He argued that Paranthropus, with its disparity in size The take-home message is that higher primates feed- between the front and back teeth, flattened premolar ing on large-husked fruits likely benefit from larger inci- and molar occlusal surfaces, and thick mandibular cor- sors to process them, whereas those that feed on smaller pora, was well suited to crushing and grinding vegeta- objects (e.g., berries, leaves) do not. Larger incisors have tion such as shoots and leaves, berries, tough wild fruits, also been argued to increase functional life given wear and grit-laden roots and bulbs. Australopithecus on the associated with increased use, though this inference has other hand, with its relatively larger front teeth and recently been called into question (see McCollum, 2007). smaller premolars and molars, at least compared with And there are caveats, such as the importance of com- Paranthropus, ‘‘would probably have had a more nearly paring closely related species; platyrrhines as a group omnivorous diet, which may have included a fair propor- have smaller incisors than do catarrhines, independent tion of flesh.’’ Robinson also recognized a fundamental of diet (Eaglen, 1984,see also Ungar, 1996). Further, the contrast in cheek tooth size between these hominins relationship between diet and incisor size in strepsir- and the ‘‘Euhomininae’’ (now Homo), observing that hines, which have specialized tooth combs, is not nearly ‘‘Telanthropus’’ and ‘‘Sinanthropus’’ had smaller molars as clear (Eaglen, 1986). Nevertheless, because relative than even Australopithecus. This fundamental contrast incisor size does track diet to an extent when comparing was echoed by Leakey et al. (1964), when these authors closely-related higher primates, there is likely value in included small molars relative to Australopithecus examining this attribute in early hominins. (including Paranthropus) as part of their revised diagno- Relative to body size, it appears that neither Australo- sis of the genus Homo in their initial description of pithecus nor Paranthropus has especially large incisors H. habilis. when compared with living apes (Ungar and Grine, Subsequent researchers attempted to better under- 1991). In fact, A. anamensis, A. afarensis,andA. africanus stand the functional implications of these differences in all fall on the regression line for a plot of I1 breadth tooth size using living primates as analogs. Groves and against body weight (in log–log space) comparing extant Napier (1968) for example, associated relatively large catarrhines (see Fig. 1). This line connects gibbons and incisors compared with molars in chimpanzees with the gorillas, suggesting that Australopithecus spp. were in- consumption of fruit with ‘‘a hard exterior but soft inte- termediate between more folivorous colobines and more rior, conditions which demand a strong incisor bite but frugivorous cercopithecoids and hominoids in their relatively little chewing.’’ They noted that, in contrast, propensity for anterior tooth use (Teaford and Ungar,

Yearbook of Physical Anthropology DIETS OF PLIO-PLEISTOCENE HOMININS 49 2000). Paranthropus robustus evidently had smaller inci- use for food acquisition and processing, in African Homo sors and presumably less incisor use in ingestion, with a erectus. On the other hand, interpretations of incisor al- residual value similar to those of many living colobines lometry in hominins should probably be approached with and modern humans. Interestingly, Homo habilis and caution, if not skepticism, given extremely small samples H. rudolfensis may have had larger incisors, more like and uncertain body weight estimates (Ungar et al., those of chimpanzees and orangutans, whereas H. erec- 2006a). We can count the number of I1s reported for tus incisors were apparently similar in size to those of some hominin taxa with the fingers of one hand, which Australopithecus (Teaford et al., 2002). presents a formidable challenge given typical size varia- These results at first glance might suggest an increase tion of about 620% for hominoids (Plavcan, 1990). An in incisor use in the earliest members of our genus, fol- even greater challenge is the paucity of associated cra- lowed by a decrease, perhaps related to increasing tool niodental and postcranial remains upon which to base body weight estimates and the huge confidence intervals of those estimates published for most early hominin taxa (Smith, 1996).

Molar allometry Studies of molar allometry are not in much better shape. In fact, not only are samples small for some taxa and body weight estimates questionable, but the rela- tionship between relative cheek-tooth size and diet is less clear. Nevertheless, molar size continues to be con- sidered by researchers an important proxy for adaptive zone (e.g., Wood and Collard, 1999; Leakey et al., 2001), and many have suggested a trend over time, with an increase in the australopiths followed by a decrease in the genus Homo (e.g., see Brace et al., 1991; McHenry and Coffing, 2000; Teaford and Ungar, 2000; Fig. 1). Enlarged, ‘‘megadont’’ cheek teeth in Australopithecus and especially Paranthropus have been said to provide more surface area to process larger quantities of low- quality, mechanically challenging foods. While there has been debate regarding the species of Homo that began the trend toward smaller cheek tooth size (compare Wood and Collard, 1999; McHenry and Coffing, 2000), dental reduction in the genus is often related to relaxa- tion of selective pressures given increasing extraoral food processing with tools and by cooking. It has also been argued to reflect an adaptation to avoid dental crowding in a smaller jaw or to slow the rate of food processing (e.g., see Brace et al., 1991; Calcagno and Gibson, 1991; Lucas et al., 2009). Some have suggested that Australopithecus and Para- nthropus had similar diets, and that tooth size differen- ces actually relate to differences in body size. Pilbeam Fig. 1. Dental allometry. Incisor sizes (above) and megadon- and Gould (1974) argued, based on positive allometry of tia quotients (below) of Plio-Pleistocene hominins. Data from cheek tooth surface area across mammals, that the aus- Coffing et al. (1994), Jungers (1988), Leakey et al. (1995), tralopiths were ‘‘scaled variants of the ‘same’ animal.’’ McHenry and Coffing (2000), Ungar and Grine (1991), and And the fact that larger-cheek-toothed species also Wood (1991). likely had larger chewing muscles suggested to some

Fig. 2. Tooth shape. Digital elevation models of M2sofAustralopithecus africanus (Stw 308) (left) and Paranthropus robustus (SKX 4446) (right) from point clouds with 25 lm lateral spacing.

Yearbook of Physical Anthropology 50 P.S. UNGAR comparable stresses across occlusal surfaces, which could and function in living primates however, we are probably be interpreted as consuming ‘‘more of the same’’ (Walker, best off looking to other lines of evidence, such as occlu- 1981; Demes and Creel, 1988). Indeed, some even advo- sal morphology, to infer the diets of fossil hominins. cated a single-species hypothesis for the South African australopiths, with variation in tooth size resulting from larger individuals having disproportionately larger mas- OCCLUSAL MORPHOLOGY ticatory apparatus (Wolpoff, 1974). Relationships between occlusal morphology and diet That said, cheek tooth areas do not scale with positive have been considered on two distinct levels, correspond- allometry for species with similar diets; they scale iso- ing to Butler’s (1983) internal and external environment, metrically with body size (Kay, 1975,Corruccini and Hen- and reflected in Evans and Sanson’s (2006) geometry of derson, 1978,Goldstein et al., 1978). In fact, while cheek occlusion and geometry of function. On one level, the oc- teeth scale isometrically, smaller animals actually pro- clusal surface has been thought of as a guide for chew- cess more food in a given period time because they chew ing, as its shape limits masticatory movements when more quickly, which makes sense given their typically opposing teeth enter and exit centric occlusion (Simpson, higher metabolic rates (Fortelius, 1988). Discussions of 1933; Crompton and Sita-Lumsden, 1970). Kay and Hiie- scaling-related metabolic equivalence of australopith mae (1974) noted for example, that insectivorous prima- cheek teeth are made moot however, by the fact that tes have reciprocally concave blades well suited to shear- there is little evidence for consistent differences in body ing tough insect chitin between the leading edges of size between these hominins (e.g., Jungers, 1988; crown crests, whereas frugivores have molars with cusp McHenry, 1988). tips more in line with the occlusal plane for crushing Cheek tooth size differences among early hominins are and grinding three-dimensional fruit flesh and seeds (see therefore likely related to food differences. They might also Rosenberger and Kinzey, 1976; Seligsohn and Sza- be related to food quantity and quality as mentioned lay, 1978). Today some dental biomechanists speak of above, or as Lucas (2004) has argued, to external proper- ‘‘autocclusal mechanisms’’ (Mellett, 1985) rather than ties of foods, such as the size, shape, or abrasiveness of teeth guiding jaw movements per se; tall cusps fit into ingested particles. A diet dominated by smaller items, deep basins are likely to prevent much transverse move- such as grass seeds or berries, or thinner ones, such as ment between teeth in occlusion (grinding). Another leaves, should select for larger teeth to increase the example would be opposing blades with acute angles of probability of fracture. Likewise, abrasive foods, such as bevel, or rake angles, which push foods away from plant parts rich in phytoliths or adherent grit, should opposing blades as they shear, resulting in forces press- select for larger teeth to increase surface area for wear. ing those blades together in ‘‘autoalignment’’ as they Thus, more megadont hominins may have been adapted approach one another (Evans and Sanson, 2006). to consume more small, thin, and/or abrasive foods. Researchers have recently begun to think of dental We may be able to gain further insights by considering functional morphology on another level though, consider- relationships between occlusal surface area and diet in ing teeth not merely as guides for chewing, but as com- living primates. Because leaves, especially mature ones, plex surfaces that interact directly with foods to accom- are tough, thin sheets requiring thorough chewing, they plish fracture (Lucas, 2004). Mammals chew to facilitate should select for larger teeth; and folivores do have lon- the assimilation of stored energy in foods. They rupture ger molars than closely-related frugivores for many pri- protective casings such as plant cell walls and insect mate groups (Kay, 1977; Vinyard and Hanna, 2005). This exoskeletons to release nutrients, and fragment items to does not hold for Old World monkeys however; colobines increase surface area for digestive enzymes to act on. As have smaller molars than cercopithecines (Kay, 1977). It Aristotle noted more than two millennia ago in De Parti- is also unclear why for many primate species, males bus Animalium, ‘‘teeth have one invariable office, have relatively smaller cheek teeth than females namely the reduction of food.’’ Workers who take this (Harvey et al., 1978). Because relative molar size does approach to dental functional morphology prefer not to not track broad diet category the same way in all groups think of teeth in terms of shearing, crushing, and grind- of extant primates, we are on shaky ground using this ing but, rather, as tools for generating and propagating attribute to retrodict food preferences for fossil taxa (see cracks through food items (Lucas and Teaford, 1994). Kay and Cartmill, 1977), at least until we can explain Because different foods have different fracture proper- differences in patterns between extant higher-level taxa. ties, they require different tools to break them efficiently, So what might explain the unexpected results for cer- and food science offers valuable predictions for tooth copithecoids? Perhaps the tendency toward smaller teeth form–function relationships (see Lucas, 2004; Lucas in colobines relates to the need to avoid dental crowding et al., 2008a; Ungar and Lucas, 2010 for review). Some given shorter faces. Of course, there remains then the foods are protected by stress-limited defenses. They tend question of whether tooth size drives jaw length or to be strong and stiff, demanding substantial force per whether it is the other way around (Brace et al., 1991). unit area to initiate a crack in them. These items are Perhaps there is a modular developmental link between also often brittle, requiring little work to spread a crack jaw length and molar size (see Vinyard and Hanna, once it starts. Examples include many nuts and other 2005). Indeed, Workman et al. (2002) found for mice that hard (in the vernacular sense) objects. Such foods should many quantitative trait loci affecting tooth size and jaw select for blunt, dome-shaped cusps to concentrate force shape are the same. This may have implications for fos- on a small area, but at the same time protect the tooth sil hominins, for which associations between jaw length itself from fracture. These cusps should oppose concave and tooth size have been noted for some time (Sofaer, surfaces formed by basins or staggered cusps to prevent 1973). And as McCollum and Sharpe (2001) have argued, energy loss due to spread or movement of food. Other there is likely a developmental link between tooth form foods are protected by displacement limited defenses and and skull form in early hominins. Until we have a better are tough or ductile. Initiating a crack in such items understanding of relationships between cheek tooth size may be less of a problem than propagating it. Examples

Yearbook of Physical Anthropology DIETS OF PLIO-PLEISTOCENE HOMININS 51 include many leaves, insect exoskeletons, and raw verte- shearing crests. There are nevertheless apparent differ- brate flesh. Such foods are best divided using offset ences among hominins. Wallace (1975) suggested for opposing blades or crests. These serve as wedges to cre- example, that among South African australopiths, Para- ate tension at the tips of advancing cracks; and there is nthropus had lower cheek tooth cusps than Australopi- little risk of cracking sharp cusp tips on tough, pliant thecus, and according to Grine (1981), the latter have foods that spread and produce compressive stress on the molars with steeper wear facets than do the former. teeth. Yet other foods are intermediate in their fracture Grine opined based on this that the ‘‘gracile’’ australo- properties, and many are composites with individual piths evinced more shearing, with occlusal surfaces slid- parts varying in their mechanical defenses. These can ing past one another nearly parallel to their planes of select for teeth intermediate in form, those with two or contact, whereas the ‘‘robust’’ form had a shallower more distinct functional elements, or differentiation of approach into and out of centric occlusion for more tooth types along the dental row. grinding, which includes both perpendicular and parallel Studies of dental morphology confirm these predic- components to occlusal contact. Dental topographic anal- tions. Folivorous and insectivorous primates generally ysis of these taxa confirm differences in molar morphol- have longer shearing crests relative to tooth length than ogy, with P. robustus having lower average occlusal sur- do frugivores, and hard-object feeders tend to have very face slope values than A. africanus at any given stage of short crests and more bulbous cusps (Rosenberger and wear (Ungar, 2007a; Fig. 2). This is consistent with the Kinzey, 1976; Kay and Covert, 1984; Strait, 1993; Mel- idea that Paranthropus was adapted to consume more drum and Kay, 1997). That said, comparisons should be hard-brittle foods than was Australopithecus. limited to closely related species as noted above for inci- Differences in occlusal form between the australopiths sor allometry studies as, for example, cercopithecoids and early Homo species have also been suggested. While have longer crests than platyrrhines independent of diet early members of our genus did not have long, sharp (Kay and Ungar, 1997; Ungar, 2005). crests as seen in extant folivorous primates, their cheek The fact that teeth change shape as they wear must teeth do appear less bunodont than those of their aus- also be considered. The gold standard for characterizing tralopith predecessors and contemporaries (Teaford primate molar crest or blade lengths has been Kay’s et al., 2002,Wood and Strait 2004). And this too has been (1977) shearing quotient (SQ) method, which involves confirmed by dental topographic analysis. Results of measurement of mesiodistal crests running up and over comparisons of dental topography of M2s of a combined cusps. Most SQ studies have been limited to unworn or sample of H. habilis, H. rudolfensis, and H. erectus with nearly unworn specimens because the cusp tips used to Australopithecus afarensis and extant chimpanzees and define crest endpoints are obliterated with wear. This gorillas indicate that early Homo as a group falls can be a problem for taxa represented mostly by worn between the two African apes in average surface slope teeth. The entire published assemblage of South African and topographic relief for all but the most worn speci- australopiths for example, includes fewer than 10 mens, and relief is significantly less than that of gorillas. unworn M2s (the tooth most often used in SQ studies). It On the other hand, the average occlusal slope for early also gives us only part of the picture. Surely natural Homo is significantly greater than that for A. afarensis. selection does not stop when wear starts; teeth should These results suggest, with caveats for small sample evolve to be worn in a manner that keeps them function- sizes and combined species samples, that early Homo ally efficient throughout the reproductive years (see species, while not specialists by any stretch of the imagi- King et al., 2005). nation, would have been capable of shearing tough foods Dental topographic analysis was developed as a land- more efficiently than could A. afarensis. The australopith mark-free approach to characterizing functionally rele- molars on the other hand, would probably have been vant aspects of occlusal morphology in variably worn more capable of resisting fracture under heavy stress teeth (Ungar and Williamson, 2000; Ungar and loads. M’Kirera, 2003; Dennis et al., 2004). We use a laser scanner to generate point clouds representing the occlu- sal table of a tooth and geographic information systems ENAMEL DEFENSES (GIS) software to interpolate and analyze the surface. Cusps are represented by mountains, fissures by valleys, Teeth and food are in a perpetual ‘‘death match’’ etc. and the tools available for measuring those surfaces (Ungar, 2008) as nature selects for resistance to fracture are used to generate data on average surface slope, an- in both; teeth must break foods without themselves gularity, relief, and other attributes. Teeth are scored for being broken. With few exceptions (notably for many pri- gross wear using Scott’s (1979) technique, and taxa are mates, fleshy fruits), it does a plant or animal little good compared by wear stage using a factorial ANOVA model. to have its parts eaten. Structural defenses not only pro- Results to date have been consistent with expectations. tect foods, but can make teeth vulnerable to breakage, While primate teeth get flatter when worn (Dennis especially given heavy stresses associated with crushing et al., 2004), folivorous monkeys and apes have, at given hard items, or the risk of fatigue failure with repetitive stages of gross wear, steeper sloping surfaces with loading of tough ones. Teeth can be protected in the greater occlusal relief than do closely related frugivores same ways that food items are defended, by hardening (M’Kirera and Ungar, 2003; Ungar and M’Kirera, 2003; (sensu Lucas et al., 2000) to prevent cracks from starting Ungar and Bunn, 2008; Bunn and Ungar, 2009). or toughening to stop cracks from spreading (see Tea- Few studies have considered variation in occlusal ford, 2007b for review). Researchers have long consid- functional morphology among early hominins. While ered the role of enamel thickness in resisting tooth frac- these species can be distinguished on the basis of their ture, and recent studies have focused on relationships occlusal form (see Bailey and Wood, 2007 and references between degree of mineralization and hardness, and therein), it is difficult to measure their SQs even on between microstructure (especially the layout of prisms) unworn molars, given bulbous cusps that lack discrete and toughness.

Yearbook of Physical Anthropology 52 P.S. UNGAR

Fig. 3. Tooth structure. A) Cross section of Homo erectus (KNM-ER 3733); B) enamel microstructure in Paranthropus boisei (KMN-ER 15940b); C) prism layout and plane of decussation; D) wriggiling and weaving of prisms in Archaeolemur majori. A and B courtesy of Fred Grine, C modified from Ungar (2010), and D courtesy of Gary Schwartz.

Enamel thickness 1995). This makes sense because tooth crowns are bilay- ered with stiff enamel overlaying more compliant dentin. Thick tooth enamel has traditionally been considered Hard-object feeders should have thicker enamel because an important signpost along our evolutionary path mark- heavy loads would make thin coats more prone to flex ing the transition from an ape-like, arboreal lifestyle to and cause tensile stresses leading to cracks in teeth a terrestrial, human-like one (e.g., Robinson, 1956). (Lucas et al., 2008b). An increase in the relative contri- Simons and Pilbeam (1972) suggested that this trait is bution of enamel to a crown should therefore result in an adaptation to lengthen the use life of the dentition less deformation for a given load and less risk of fracture given rapid wear with the consumption of tough, grit- (Popowics et al., 2001). laden foods on the ground (see also Macho and Spears, Despite methodological differences in measurement, 1999). While this seems intuitive, there is, as Kay (1981) there has been recognition by many that not only do has noted, no tendency among living apes or Old World Plio-Pleistocene hominins have thicker molar enamel monkeys for more terrestrial species to have thicker than extant African apes, but that fossil species vary enamel than do more arboreal ones. And the fact that from one another. Wallace (1975) wrote that compared the largely arboreal orangutan not only has thicker with australopiths, early Homo specimens from Swartk- enamel but also tends to have less worn teeth than rans and those he examined from Koobi Fora seemingly the more terrestrial gorilla, suggests that this need have thinner enamel (see Fig. 3). Beynon and Wood’s not be a compensatory mechanism for increased wear (1986) study of naturally fractured specimens support (Dean et al., 1992). this observation, confirming that Paranthropus boisei Thickened enamel in early hominins could instead be has thicker molar enamel than early Homo, especially an adaptation for structural reinforcement to prevent H. erectus. Further, Grine and Martin (1988) found for a fracture (Kay, 1981). Indeed, primates that consume small sample of sectioned teeth that both P. robustus hard objects tend to have thicker molar enamel than do and P. boisei had thicker enamel than Australopithecus closely related species that eat softer foods (Dumont, africanus, suggesting to them functional implications for

Yearbook of Physical Anthropology DIETS OF PLIO-PLEISTOCENE HOMININS 53 countering increased wear and/or occlusal loads (but see review). Most mammals bundle thousands of long, thin Olejniczak et al., 2008a). crystallites, each about 40 nm in diameter, into cylindri- But the relationship between enamel thickness and cal or semicylindrical prisms or rods like bunches of diet is not a simple one. It is more likely that the distri- dried spaghetti strands. These prisms, each between bution of enamel across a crown, not just its average about 2–10 lm in diameter, are packed together and run thickness, is important to understanding function (e.g., from the EDJ to the surface of the tooth (see Fig. 3). In Greaves, 1973; Rensberger, 1973; Macho and Thackeray, primates, individual prisms tend to run parallel to one 1992; Schwartz, 2000). Dental sculpting provides a case- another as they approach the surface; we call this radial in-point. Many mammals have teeth with what Fortelius enamel. But the angle at which they hit the outer sur- (1985) has referred to as ‘‘secondary morphology;’’ they face of the crown varies which, according to Shimizu actually require wear to function properly (see Ungar, et al. (2005), should effect both wear resistance and stiff- 2010 for discussion). Because enamel is harder than den- ness of the tissue and therefore have implications for tin, wear can cause a sharp edge to form where the two surface wear and strength. tissue types meet on the occlusal surface (Shimizu, 2002; It is also important to consider the paths of prisms as Ungar and M’Kirera, 2003; Kono, 2004). Thinner enamel they make their way from the EDJ to the crown surface. can mean quicker dentin exposure to facilitate fracture Depending on the directions and magnitudes of forces of tough foods. Thus, the morphology of the enamel–den- acting during mastication, radial enamel is susceptible tin junction (EDJ) can literally guide wear to sculpt oc- to fracture with cleavage along planes of weakness clusal surfaces. between adjacent rows. Decussation, wherein layers of New studies using X-ray microcomputed tomography prisms wiggle about along their long axes, can mitigate (micro-CT) to map the distribution of enamel across this problem; changing prism directions require cracks tooth crowns show great promise to help us better to change direction as they spread, increasing the work understand both dental form and function (e.g., Kono, required for fracture. Further, adjacent layers can be 2004; Gantt et al., 2006; Kono and Suwa, 2008; Olejnic- interwoven with one another at angles up to about 908 zak et al., 2008b; Smith and Tafforeau, 2008). For exam- to form Hunter–Schreger (H–S) bands, which can be ple, australopiths appear to have especially thick enamel stacked horizontally, vertically, or in a zigzag fashion. over the cusp tips and relatively short dentin horns, These H–S bands stop cracks by absorbing the energy whereas humans have thicker enamel at cusp bases required for their propagation. Enamel can be further (Olejniczak et al., 2008a). Olejniczak et al. (2008a) sug- strengthened when different enamel types (e.g., radial, gest that the australopith pattern reflects the consump- horizontal, vertical, and zigzag) are themselves layered tion of abrasive small objects, or relates to the preven- to form complex schmelzmuster patterns (see Maas and tion of cracks at the EDJ in large-object feeders (see Dumont, 1999). Lucas et al., 2008b). They also relate the pattern seen in Researchers have recently begun to consider the impli- H. sapiens to distribution of masticatory forces (see cations of enamel microstructure for diet in early homi- Macho and Spears, 1999). nins. Macho and Shimizu (2009) for example, compared the angle at which enamel prisms approach the occlusal Enamel mineral content surface in Paranthropus robustus and Australopithecus africanus, and argued that the ‘‘robust’’ australopith Researchers are beginning to consider the fracture cheek teeth are stiffer and adapted to more vertical properties of enamel at a finer scale, using nanoindenta- loads, whereas those of the ‘‘gracile’’ australopiths are tion to study hardness and examining histology to map more wear resistant and adapted to coping with more prism layout and resistance to crack propagation. Nano- laterally directed loads. Macho and Shimizu (2010) also indentation studies indicate that hardness and stiffness considered prism orientation in A. anamensis, which vary across primate enamel crowns (Cuy et al., 2002; suggested to them that this hominin was adapted to Braly et al., 2007; Lee et al., 2010). This research has tough foods requiring a significant shear component and shown that indentation hardness and Young’s modulus a wide range of loading directions. can decrease by more than 50% from the occlusal surface Functional studies of hominin enamel decussation to the EDJ. These attributes also vary between buccal have thus far been limited. Beynon and Wood (1986) and lingual sides of a tooth and between teeth (Darnell suggested in their study that Paranthropus had little et al., 2010). According to Braly et al. (2007), changes in enamel decussation, but that early Homo had more. enamel properties at this scale relate to local chemistry Grine and Martin (1988) on the other hand, observed (levels of mineralization, organic matter, and water con- well-developed H–S bands in Paranthropus enamel, and tent) and varying volume fractions of inorganic crystals argued that prism decussation in these hominins func- and organic matrix. While there has yet to be a study of tioned in stopping cracks. Macho et al. (2005) and Macho enamel hardness and mineral content in fossil hominins, and Shimizu (2010) also documented decussation in Aus- researchers are beginning to document variation in in- tralopithecus anamensis, especially close to the EDJ dentation hardness and Young’s modulus within teeth of where, according to Lucas et al. (2008), cracks are prone different primate species (Darnell et al., 2010). Such to start. But studies to date have been limited to exposed studies may in the future provide new insights into rela- surfaces on naturally broken specimens or a few sec- tionships between dental form and function. tioned teeth and, as Macho et al. (2005) have noted, it is the complex three-dimensional arrangement of prisms Enamel microstructure across a tooth that is likely to be most informative. In this light, new technologies, such as phase contrast X- While enamel histology has little effect on hardness or ray synchrotron microtopography, which allows whole- stiffness at nanoscales (Braly et al., 2007), the internal tooth imaging with submicron resolution (Tafforeau and structure of this tissue can be very effective at limiting Smith, 2008), may help us realize the potential of func- the spread of cracks (see Maas and Dumont, 1999 for tional studies of enamel microstructure.

Yearbook of Physical Anthropology 54 P.S. UNGAR DIRECT EVIDENCE OF TOOTH USE: stresses. If these in vitro tests are reasonable proxies for ANTEMORTEM DAMAGE AND WEAR in vivo conditions, this new tool may well allow recon- structions of maximum bite forces by early hominins and While tooth size, shape, and structure likely reflect di- lead to insights into very rarely consumed items. Con- etary adaptations, they tell us more about potential than sistent criteria for antemortem chip identification and what a specific animal in the past ate on a daily basis. reporting, and more comparisons with other taxa will As Kinzey (1978) asked rhetorically, ‘‘is it possible that hopefully also lead to further insights. features of the dentition are selected for on bases other than the ‘primary specialization’?’’ Perhaps, as he specu- lated, ‘‘when a food item is critical for survival, even Dental microwear though not part of the primary specialization, it will One of the best approaches to reconstructing diets of influence the selection of dental features.’’ As Robinson early hominins is dental microwear analysis. Scratches and Wilson (1998) later noted, ‘‘some resources are and pits form on a tooth’s surface as the result of its use intrinsically easy to use and are widely preferred, while and so provide direct evidence for diet. Microwear fea- others require specialized phenotypic traits on the part tures are like footprints in the sand, traces left by real of the consumer. This asymmetry allows optimally forag- actions of specific individuals at a moment in time. They ing consumers to evolve phenotypic specializations on are a direct connection to animals that lived in the past. nonpreferred resources without greatly compromising Most studies of dental microwear have focused on inci- their ability to use preferred resources.’’ They referred to sors and molars. the notion that animals may actually avoid the foods to which they are adapted when more favored ones are Incisor microwear. Incisor microwear tells us some- available as Liem’s Paradox. thing about front tooth use. It has been examined in a Chimpanzees and gorillas provide a useful example. broad range of mammals, from kangaroos to moose These apes differ markedly in dental allometry, morphol- (Young, 1986; Young et al., 1990). Work on living prima- ogy, and microstructure, to say nothing of diet-related tes suggests that habitual incisor use in food preparation differences in their jaws, chewing muscles, and guts. De- results in relatively high densities of microwear features spite this, as Wrangham (2007) has noted, the two ‘‘have on front teeth (e.g., Kelley, 1990; Ungar, 1990, 1994). closely similar diets. Both choose ripe fruits when they Some have also argued that microwear feature types can are available, being almost equally frugivorous.’’ Gorillas be associated with specific ingestive behaviors, such as exhibit Liem’s Paradox; notwithstanding clear adapta- horizontally oriented scratches and stripping of foods lat- tions for tough, fibrous foods, they prefer soft, sugary erally across the mouth (Walker, 1976; Ryan, 1981, fruits given the choice (Remis 2002). The African apes 1994). It may even be that incisor microwear patterning differ in diet mostly at times of resource scarcity when, reflects substrate use, with predominant dietary abra- as Wrangham (2007) notes, ‘‘gorillas can survive by eat- sives encountered on or near the ground (exogenous grit) ing fibrous foods for 100% of their feeding time. Chim- causing different wear feature incidences or sizes than panzees never do so.’’ Perhaps then, unique aspects of those encountered high in the trees (phytoliths) (Walker, tooth shape and structure in early hominins likewise 1976; Ungar, 1994). reflect nonpreferred foods (Ungar, 2004; Constantino A few studies have documented incisor microwear in et al., 2009). But how would we know? We can look to Plio-Pleistocene hominins. Ryan and Johanson (1989) nongenetic clues, evidence of actual use of teeth, such as suggested that Australopithecus afarensis had a mosaic antemortem chipping and dental microwear (Ungar, of gorilla-like and baboon-like features reflecting the use 2009). of these teeth to strip gritty plant parts such as roots and rhizomes. And Ungar and Grine (1991) noted that Antemortem damage: Tooth chipping A. africanus had a higher average incisor microwear fea- ture density than P. robustus, suggesting the ‘‘gracile’’ Robinson (1954) claimed that Paranthropus robustus australopiths ate more abrasive foods requiring anterior had more chipped teeth than Australopithecus africanus. tooth use in ingestion than did the ‘‘robust’’ species. He attributed the difference to consumption of grit-laden roots and bulbs by the ‘‘robust’’ australopiths. According Molar microwear. Molar microwear tells us something to Tobias (1967) however, the two species had dental about the fracture mechanics of foods, especially as they chips ‘‘similar in size, character, and number per jaw’’; relate to movements of opposing tooth surfaces relative and all were rather large, suggesting to him bouts of to one another during mastication. This falls under the bone chewing. Wallace (1975) later also examined ante- domain of what engineers call tribology (Schulz et al., mortem dental chipping in these hominins and, like 2010). When stress-limited (e.g., hard-brittle) foods are Tobias, found no notable differences between A. africa- crushed between molars, they tend to form pits, whereas nus and P. robustus. He reasoned that this indicates sim- displacement-limited (e.g., tough-pliable) items sheared ilar amounts of grit in the diets of ‘‘gracile’’ and ‘‘robust’’ between blades or crests are apt to cause scratches as australopiths. opposing teeth slide past one another, dragging food- Antemortem tooth chipping in early hominins has borne abrasives between them (see Teaford, 1988, 2007a; recently been revisited by paleoanthropologists. Grine et Ungar et al. 2007b for review). Smaller pits can also al. (2010) reported similar chip rates between premolars result from the consumption of tough foods as prisms and molars of A. africanus, suggesting to them that are ‘‘plucked’’ from their surrounding matrix due to fric- chewing stresses did not differ substantially between the tion (Teaford and Runestad, 1992). Thus, microwear fea- two tooth types. Constantino et al. (2010) have taken ture size can also help inform us of the material proper- tooth chipping evidence a step further, with in vitro ties of foods. And relationships between microwear and experiments with human molars and Vickers indenta- diet seem to hold well not just for primates, but across tions suggesting that chip dimensions reflect chewing Mammalia, from antelopes to zebras, bats to moles, pigs

Yearbook of Physical Anthropology DIETS OF PLIO-PLEISTOCENE HOMININS 55

Fig. 4. Tooth microwear. Three-dimensional axiomatic representations of Facet 9 of Australopithecus africanus (Sts 53) (top) and Paranthropus robustus (SK 42) (bottom). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary. com.] to sheep, cats to dogs, marsupials to primates, and other ent microhabitats and those sampled in different seasons taxa (see Ungar, 2010). (e.g., Teaford and Robinson, 1989, e.g., Teaford and Glan- There have been several studies of molar microwear in der, 1996; Nystrom et al., 2004; Teaford et al., 2006). early hominins. Grine (1986) found Australopithecus The most common technique for quantifying high-reso- africanus occlusal surfaces to be dominated by micro- lution microwear patterns has involved imaging by scan- wear scratches, while those of Paranthropus robustus ning electron microscopy followed by user identification had more pits (see Fig. 4). He attributed this difference and measurement of individual scratches and pits to the consumption of small, hard objects by the ‘‘robust’’ (Ungar et al., 1991, 1995). This approach has provided australopiths and softer foods, such as fruits and imma- remarkable results, especially given intra- and interob- ture leaves, by the ‘‘gracile’’ hominins. Subsequent work server error in microwear feature measurement (Grine on A. afarensis and A. anamensis showed that these et al., 2002). Still, a newer technique combining white- ‘‘gracile’’ australopiths also had microwear surfaces light confocal microscopy with scale-sensitive fractal dominated by striations, with remarkable consistency analysis offers more automated surface texture charac- over time and between inferred habitat types (Grine terization, and is becoming increasingly popular (Ungar et al., 2006a,b). This suggested that specimens of Austa- et al., 2003, 2007b; Scott et al., 2006). Species with more lopithecus spp. examined more likely consumed tough pitting tend to have more complex surfaces (defined by foods than hard-brittle ones in the days or weeks before change in roughness with scale of observation); whereas death. Grine et al. (2006a,b) concluded that these species those with more aligned striations tend to have higher were probably not hard-object specialists despite ana- surface anisotropy. Other texture attributes, such as fill tomical traits suggesting potential to consume such volume and the scale of maximal complexity, can be items. Early Homo specimens examined have somewhat related to feature sizes (see Scott et al. 2006 for details). higher average pit percentages than Australopithecus Folivorous primates tend to have low complexity and spp., though their surfaces were still not dominated by high anisotropy values, those that consume hard-brittle pits (Ungar et al., 2006b). This suggested to Ungar et al. foods more often have high complexity and low anisot- (2006b) a preference for less fracture resistant foods, ropy, and frugivores often have intermediate or varied though small pits in H. erectus and Homo from Swartk- texture attributes (Ungar et al., 2007b). rans Member 1 hint that these hominins may have con- While there is general congruence between feature- sumed more hard or tough items prior to death than did based and texture-based microwear analyses, the latter H. habilis and Homo from Sterkfontein Member 5C. promises even more resolving power because it is free from observer measurement error. Reduced noise in New approaches to microwear analysis. As research measurements gives us more confidence to consider into the etiology of microscopic use-wear on teeth has subtleties in our data, such as the distribution of varia- progressed, it has become clear that this approach to tion within samples. And the ability to document varia- hominin diet reconstruction has not yet reached its full tion within a sample may be among the most valuable potential (see Rose and Ungar, 1998; Teaford, 2007a; contributions microwear has to offer. Ungar et al., 2007b). We can get well beyond ‘‘Species A Dental microwear reflects diets only days or weeks ate mostly hard-brittle foods whereas Species B ate before death because individual features on these scales mostly soft-tough ones.’’ Indeed, many years of study of are often no more than a few microns deep, and so wild primates have shown rather subtle variation in turn over quickly with further wear (Teaford and microwear patterns between individuals living in differ- Oyen, 1989). This fact, referred to as ‘‘the last supper’’

Yearbook of Physical Anthropology 56 P.S. UNGAR phenomenon (Grine, 1986), is both a liability and an It is also interesting to note that eastern African aus- asset. A record of the last few meals of an individual tralopiths lack values at the upper end of both the com- may tell us little about dietary adaptations of a species; plexity and anisotropy ranges. Extant taxa sampled to but with a sufficient sample of specimens, we might date have at least some high values in one of these two begin to look at variation in diet within that species, attributes given diets including foods with stress-limited especially if seasonal biases in death and preservation or displacement-limited defenses. The atypical pattern do not overwhelm our signals. We can predict that if seen in these hominins may relate in part to tooth hard-brittle foods are preferred, most individuals in a shape. Ungar et al. (2010, 2011) noted that high anisot- sample should have complex microwear surface textures. ropy values seen in living tough-food eaters is likely If on the other hand, such foods are fallback items taken related to constraints on tooth-tooth movement seen in when softer, weaker foods are unavailable, only a small living folivores or grass-eaters that have high cusps and percentage of specimens in a sample should have high substantial occlusal relief. While low complexity is not texture complexity. Thus, microwear could in principle consistent with hard-object feeding, low anisotropy need help us infer aspects of foraging strategy. When com- not be incompatible with a tough-food diet if items are bined with dental functional morphology, microwear ground between flat or bulbous cusps. It can also be might even offer clues as to whether individuals of a noted microwear texture analysis also hints at possible past species commonly or rarely consumed the foods to dietary variation among eastern African australopiths which they were adapted, and so offer insights into the (e.g., a broader range of scale of maximal complexity val- nature of selection (Ungar, 2009). ues in P. boisei), though not to the degree separating Dental microwear textures of Australopithecus africanus them from their South African congeners. and Paranthropus robustus provide an example (Scott Microwear textures have also been examined in Homo et al., 2005). The ‘‘gracile’’ australopith has on average habilis and H. rudolfensis (Ungar and Scott, 2009; lower microwear texture complexity (considered a proxy Ungar et al., 2011). Early Homo as a group shows mod- for food hardness) and more anisotropy (considered a erate average complexity and relatively low anisotropy. proxy for food toughness) than does the ‘‘robust’’ species. Homo erectus has lower average textural fill volume and Still, these species both have some individuals with scale of maximal complexity than H. habilis, consistent lower anisotropy and lower complexity values, perhaps with relatively more small pits and perhaps some tough implying consumption of less mechanically challenging food consumption (see above). Homo erectus also has a foods. But the distributions for A. africanus and P. remarkably high dispersion of complexity, matched robustus differ, with data points for these species spread among the hominins only by Paranthropus robustus. into the upper range of anisotropy and complexity This is consistent with a fairly broad diet, at least in respectively. This suggested to Scott et al. (2005) overlap terms of food fracture properties. in the fracture properties of foods, but differences between the australopiths in critical dietary resources Microwear and enamel mineral content and consumed periodically during the year. Indeed, the P. structure. Before we leave the discussion of microwear, robustus distribution of complexity values is similar to a few words about the effects of enamel mineral content that for a sample of Lophocebus albigena, a species and microstructure on the hardness and toughness of reported to fall back on hard bark and seeds when softer, enamel are in order, particularly given discussions preferred foods are unavailable (Lambert et al., 2004). above. Maas (1991, 1994) found in abrasion experiments Paranthropus robustus may have likewise consumed with tooth enamel and silicon carbide grits that while softer foods much of the time, with craniodental adapta- abrasive particle size was the primary determinant of tions reflecting less preferred but still critical hard, brit- microwear feature size, variation in crystallite orienta- tle foods. If so, P. robustus may present an example of tion could affect striation breadths under shearing loads. Liem’s Paradox in the hominin lineage (Ungar, 2007a, Further, Macho and Shimizu (2009) speculated that the 2009). orientation of prisms might affect microwear patterning, Eastern African australopiths have also been exam- which could complicate interpretations of results com- ined by microwear texture analysis, with some results as paring taxa with different enamel microstructures. The expected but others surprising. Australopithecus ana- extent of this effect is probably limited however; while mensis, A. afarensis, and Paranthropus boisei all have prism orientation is very important for toughening lower average texture complexity values than extant enamel against crack propagation, it has little effect on hard-object feeding primates, but at the same time, have hardness (Braly et al., 2007). On the other hand, mineral lower average anisotropy values than living folivores content can have an important effect on enamel, and (Ungar et al., 2008, 2010, 2011). Complexity results for indentation studies indicate that hardness can decrease A. anamensis and A. afarensis were not unexpected by more than 50% from the occlusal surface to the EDJ given feature-based studies suggesting limited dietary (Cuy et al., 2002). variability and a lack of hard-object feeding. On the While degree of mineralization and prism orientation other hand, the similarity of complexity results for P. could in principle affect patterns of microscopic wear, boisei with those for A. anamensis and A. afarensis is there is little evidence for an effect of sufficient magni- surprising, both because the craniodental toolkits of tude to affect interpretation, at least not on the scales at these hominins are so different, and because microwear which microwear is typically examined (Teaford, 1988). textures of P. robustus are so different. While it is possi- If there were, we would expect to see consistent varia- ble that microwear reflects a hard-object-fallback adapta- tion within primate species related to gross wear tion for the eastern African australopiths (especially P. because prism orientation and mineral content change boisei), it is hard to imagine that we are completely from the EDJ to the occlusal surface. This does not seem missing a hard-object complexity signal due to sampling to be the case. More to the point, studies of a very broad error given data for more than 30 individuals spread range of extant mammals with different enamel proper- over such substantial time and space. ties consistently confirm expected relationships between

Yearbook of Physical Anthropology DIETS OF PLIO-PLEISTOCENE HOMININS 57 microwear patterns and diet. Folivorous primates have enamel may not be so thick overall as previously thought higher anisotropy and lower complexity averages than judging from microtomographic study of A. africanus frugivores, especially hard-object feeders (Ungar et al., (Olejniczak et al., 2008a). And prism orientation in A. 2007b). Grazing bovids have higher aniostropy and lower anamensis and A. africanus may be consistent with an complexity values than browsers, especially those that ability to resist fracture given laterally-directed shearing include fruit in their diet (Ungar et al., 2007a). Grazing movements (Macho and Shimizu, 2009, 2010). Dental kangaroos also have higher anisotropy and lower com- microwear of Australopithecus spp. suggests that these plexity values than browsing wallabies (Prideaux et al., hominins did not regularly consume hard-brittle foods, 2009). And among carnivores, durophagus hyenas have though they may have consumed tough items at least higher complexity and lower anisotropy averages than occasionally (Scott et al., 2005,Ungar et al., 2010). Micro- felids, especially tough-flesh-eating cheetahs (Schubert wear also suggests variation within the genus, with the et al., 2010). The proof is in the pudding. eastern African taxa having lower average microwear complexity values than the South African species. DISCUSSION Paranthropus. The ‘‘robust’’ australopiths P. boisei and Even a cursory review of recent work on the dental P. robustus have relatively small front teeth (Kay, evidence for diets of early hominins makes clear that 1985,Ungar and Grine, 1991). If incisor allometry data 1 this is a vibrant, growing research domain. As our are accurate, the P. robustus I is within the range of understanding improves, we can begin to ask questions extant colobines relative to body weight; among the liv- like, ‘‘was selection driven by preferred foods or fallback ing apes, only humans have smaller front teeth. And the resources?’’ rather than simply, ‘‘did they eat hard low density of microwear features on P. robustus incisors objects?’’ But we clearly have a long way to go before we is consistent with their limited use in ingestion com- reach the limits of our potential knowledge. Kant’s pared with those of extant anthropoids that employ (1783) observation that, ‘‘every answer given on principle these teeth regularly to husk large fruits (Ungar and of experience begets a fresh question, which likewise Grine, 1991; Ungar, 1998). requires its answer’’ applies well to reconstructions of Paranthropus spp. have large, bulbous molar teeth early hominin diets. Rescher (1999) remarks that, ‘‘in a that could have served well in hard-object feeding. Their complex world, the natural dynamics of rational inquiry megadontia quotients are extremely high and, at least will inevitably exhibit a tropism toward increasing com- among South African early hominins, Paranthropus has plexity’’ does too. The more we learn, the more it seems the least sloping occlusal surfaces at given stages of there is to know. Despite these Sisyphean frustrations gross wear and shallowest wear facets (Grine, 1981; Tea- however, new methods and theoretical approaches are ford et al., 2002; Ungar, 2007a). The ‘‘robust’’ australo- bringing progress and improving our understandings of piths also have thick molar enamel, and may have well- the diets of Plio-Pleistocene hominins. developed H–S bands, with prisms oriented to resist ver- tical loads (Grine and Martin, 1988; Olejniczak et al., Plio-Pleistocene hominin diets 2008a; Macho and Shimizu, 2009). These features sug- gest an ability to withstand heavy stresses or fatigue A convenient way to summarize our knowledge to date failure related to repetitive loading. is to consider the Plio-Pleistocene hominins genus-by-ge- One question that has arisen is whether these dietary nus, especially because the number of analyses and specializations resulted in stenotopy, including relatively types of data available differ between species. few foods, or whether they actually reflect eurytopy, with a broadened subsistence base including both extremely Australopithecus. If dental allometry data hold, A. hard foods and less mechanically challenging items anamensis, A. afarensis, and A. africanus all have inci- (Wood and Strait, 2004). The microwear evidence is sors intermediate in relative size between those of chim- mixed in this regard. Paranthropus robustus does show panzees, orangutans, and many cercopithecines on the substantial variance in microwear texture complexity, one hand, and more folivorous colobines and humans on including some specimens suggesting consumption of the other. Their incisors are about the same relative size foods with stress-limited defenses (Scott et al., 2005). On as those of gorillas and gibbons, taxa that do not focus the other hand, no P. boisei specimens examined to date on foods requiring extensive incisal preparation (Teaford have the high-complexity microwear texture expected of and Ungar, 2000). And incisor microwear on A. africanus a hard-object feeder (Ungar et al., 2008, 2011). Rather, P. is consistent with moderate levels of incisor use (Ungar, boisei microwear suggests a softer- or tough-food diet. and Grine 1991). Still, microwear of the anterior teeth of Differences between the South African and eastern Afri- A. afarensis (Ryan and Johanson, 1989) and extreme gross can ‘‘robust’’ australopiths may indicate differences in wear on the front teeth of A. anamensis (Ward et al., their feeding strategies, consistent with variation in iso- 2010) suggest possible variation in degree and types of tope signatures reported by van der Merwe et al. (2008) ingestive behaviors among the ‘‘gracile’’ australopiths. and Cerling et al. (2011). The molar teeth of ‘‘gracile’’ australopiths are rela- tively large and bunodont, though their functional mor- Early Homo. Early Homo incisors are all over the map. phology may suggest a mosaic of adaptations for fractur- If allometry data for early Homo species are correct, ing stress-limited and displacement-limited foods. These both H. habilis and H. rudolfensis have large front teeth, hominins lack the distinct shearing crests found on the about the same size relative to body weight as living cheek teeth of many extant primates; topographic relief chimpanzees and orangutans, species known to use their of A. afarensis molars for example, is less than that of front teeth for husking large fruits and other ingestive living chimpanzees (Ungar, 2004). Further, Australopi- behaviors. The African H. erectus value is intermediate thecus spp. have thickened molar enamel compared with between those of H. habilis and H. rudolfensis on the living African apes, particularly under the cusp tips one hand, and modern H. sapiens on the other. Relative (Olejniczak et al., 2008a). On the other hand, their molar incisor size in African H. erectus falls on the regression

Yearbook of Physical Anthropology 58 P.S. UNGAR line, along with living gibbons and gorillas, which tend to evidence, such as stone tools, and the remains of plants be more limited in anterior tooth use during ingestion and animals found in hominin-bearing deposits can (Teaford et al., 2002). This might suggest the consump- also provide important clues. And studies of ecological tion of more foods requiring incisal preparation in analogs and development of energetics models can help H. habilis and H. rudolfensis compared with their aus- us put together the most complete picture possible. tralopith predecessors and contemporaries, but a decrease Finally, new approaches on the horizon, such as studies in incisor use in African H. erectus, either because of a of parasite relationships, microbial ecology, and com- change in diet, or perhaps increased extraoral food proc- parative genomics hold the promise of even better essing (Ungar et al., 2006a). Dental microwear analysis of understandings. early Homo incisors could be helpful in resolving this. Early Homo cheek teeth also vary. While Homo habilis ACKNOWLEDGMENTS and H. rudolfensis have higher megadontia quotients than living great apes (albeit lower than their Para- The author thanks Bob Sussman for his kind invita- nthropus contemporaries), H. erectus cheek teeth are as tion to submit this article to the Yearbook of Physical small or smaller (Teaford et al., 2002). While small sam- Anthropology. He also thanks Mark Teaford, Gary ple sizes preclude separate comparisons of occlusal to- Schwartz, Fred Grine, Matt Sponheimer, Paul Constan- pography between early Homo species, the group as a tino, and Dave Strait for comments and discussions whole has more sloping molar surfaces than its australo- related to this review, and Fred Grine and Gary pith predecessors, with an average value between those Schwartz for providing the images in Figure 3. of chimpanzees and gorillas, at least until late in the wear sequence. And while little work has been done on enamel strength in the earliest members of our genus, LITERATURE CITED early Homo (especially H. erectus) seems to have thinner enamel than the australopiths (Beynon and Wood, 1986). Atkins RC. 2002. Dr. Atkins’ new diet revolution. New York: Results suggest a relaxation of or change in selective Quill. pressures consistent with less hard-object feeding but Bailey SE, Wood BA. 2007. 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